Route of Sensitization to Peanut Influences Immune Cell Recruitment at Various Mucosal Sites in Mouse: An Integrative Analysis

Symptom occurrence at the first ingestion suggests that food allergy may result from earlier sensitization via non-oral routes. We aimed to characterize the cellular populations recruited at various mucosal and immune sites after experimental sensitization though different routes. BALB/cJ mice were...

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Main Authors: Mélanie Briard, Marine Guinot, Marta Grauso, Blanche Guillon, Stéphane Hazebrouck, Hervé Bernard, Grégory Bouchaud, Marie-Laure Michel, Karine Adel-Patient
Format: Article
Language:English
Published: MDPI AG 2022-02-01
Series:Nutrients
Subjects:
Online Access:https://www.mdpi.com/2072-6643/14/4/790
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author Mélanie Briard
Marine Guinot
Marta Grauso
Blanche Guillon
Stéphane Hazebrouck
Hervé Bernard
Grégory Bouchaud
Marie-Laure Michel
Karine Adel-Patient
author_facet Mélanie Briard
Marine Guinot
Marta Grauso
Blanche Guillon
Stéphane Hazebrouck
Hervé Bernard
Grégory Bouchaud
Marie-Laure Michel
Karine Adel-Patient
author_sort Mélanie Briard
collection DOAJ
description Symptom occurrence at the first ingestion suggests that food allergy may result from earlier sensitization via non-oral routes. We aimed to characterize the cellular populations recruited at various mucosal and immune sites after experimental sensitization though different routes. BALB/cJ mice were exposed to a major allergenic food (peanut) mixed with cholera toxin via the intra-gastric (i.g.), respiratory, cutaneous, or intra-peritoneal (i.p.) route. We assessed sensitization and elicitation of the allergic reaction and frequencies of T cells, innate lymphoid cells (ILC), and inflammatory and dendritic cells (DC) in broncho-alveolar lavages (BAL), lungs, skin, intestine, and various lymph nodes. All cellular data were analyzed through non-supervised and supervised uni/multivariate analysis. All exposure routes, except cutaneous, induced sensitization, but intestinal allergy was induced only in i.g.- and i.p.-exposed mice. Multivariate analysis of all cellular constituents did not discriminate i.g. from control mice. Conversely, respiratory-sensitized mice constituted a distinct cluster, characterized by high local inflammation and immune cells recruitment. Those mice also evidenced changes in ILC frequencies at distant site (intestine). Despite absence of sensitization, cutaneous-exposed mice evidenced comparable changes, albeit less intense. Our study highlights that the initial route of sensitization to a food allergen influences the nature of the immune responses at various mucosal sites. Interconnections of mucosal immune systems may participate in the complexity of clinical manifestations as well as in the atopic march.
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spelling doaj.art-66786ba6b7e1441d927b2719fde57d882023-11-23T21:28:26ZengMDPI AGNutrients2072-66432022-02-0114479010.3390/nu14040790Route of Sensitization to Peanut Influences Immune Cell Recruitment at Various Mucosal Sites in Mouse: An Integrative AnalysisMélanie Briard0Marine Guinot1Marta Grauso2Blanche Guillon3Stéphane Hazebrouck4Hervé Bernard5Grégory Bouchaud6Marie-Laure Michel7Karine Adel-Patient8Département Médicaments et Technologies pour la Santé (DMTS), Université Paris-Saclay, CEA, INRAe, Service de Pharmacologie et d’Immunoanalyse, 91190 Gif-sur-Yvette, FranceDépartement Médicaments et Technologies pour la Santé (DMTS), Université Paris-Saclay, CEA, INRAe, Service de Pharmacologie et d’Immunoanalyse, 91190 Gif-sur-Yvette, FranceDépartement Médicaments et Technologies pour la Santé (DMTS), Université Paris-Saclay, CEA, INRAe, Service de Pharmacologie et d’Immunoanalyse, 91190 Gif-sur-Yvette, FranceDépartement Médicaments et Technologies pour la Santé (DMTS), Université Paris-Saclay, CEA, INRAe, Service de Pharmacologie et d’Immunoanalyse, 91190 Gif-sur-Yvette, FranceDépartement Médicaments et Technologies pour la Santé (DMTS), Université Paris-Saclay, CEA, INRAe, Service de Pharmacologie et d’Immunoanalyse, 91190 Gif-sur-Yvette, FranceDépartement Médicaments et Technologies pour la Santé (DMTS), Université Paris-Saclay, CEA, INRAe, Service de Pharmacologie et d’Immunoanalyse, 91190 Gif-sur-Yvette, FranceINRAe, UR1268 Biopolymères, Intéractions et Assemblages (BIA), 44316 Nantes, FranceMicalis Institute, INRAE, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, FranceDépartement Médicaments et Technologies pour la Santé (DMTS), Université Paris-Saclay, CEA, INRAe, Service de Pharmacologie et d’Immunoanalyse, 91190 Gif-sur-Yvette, FranceSymptom occurrence at the first ingestion suggests that food allergy may result from earlier sensitization via non-oral routes. We aimed to characterize the cellular populations recruited at various mucosal and immune sites after experimental sensitization though different routes. BALB/cJ mice were exposed to a major allergenic food (peanut) mixed with cholera toxin via the intra-gastric (i.g.), respiratory, cutaneous, or intra-peritoneal (i.p.) route. We assessed sensitization and elicitation of the allergic reaction and frequencies of T cells, innate lymphoid cells (ILC), and inflammatory and dendritic cells (DC) in broncho-alveolar lavages (BAL), lungs, skin, intestine, and various lymph nodes. All cellular data were analyzed through non-supervised and supervised uni/multivariate analysis. All exposure routes, except cutaneous, induced sensitization, but intestinal allergy was induced only in i.g.- and i.p.-exposed mice. Multivariate analysis of all cellular constituents did not discriminate i.g. from control mice. Conversely, respiratory-sensitized mice constituted a distinct cluster, characterized by high local inflammation and immune cells recruitment. Those mice also evidenced changes in ILC frequencies at distant site (intestine). Despite absence of sensitization, cutaneous-exposed mice evidenced comparable changes, albeit less intense. Our study highlights that the initial route of sensitization to a food allergen influences the nature of the immune responses at various mucosal sites. Interconnections of mucosal immune systems may participate in the complexity of clinical manifestations as well as in the atopic march.https://www.mdpi.com/2072-6643/14/4/790food allergypeanutroutes of exposureBALB/c micecellular immune response
spellingShingle Mélanie Briard
Marine Guinot
Marta Grauso
Blanche Guillon
Stéphane Hazebrouck
Hervé Bernard
Grégory Bouchaud
Marie-Laure Michel
Karine Adel-Patient
Route of Sensitization to Peanut Influences Immune Cell Recruitment at Various Mucosal Sites in Mouse: An Integrative Analysis
Nutrients
food allergy
peanut
routes of exposure
BALB/c mice
cellular immune response
title Route of Sensitization to Peanut Influences Immune Cell Recruitment at Various Mucosal Sites in Mouse: An Integrative Analysis
title_full Route of Sensitization to Peanut Influences Immune Cell Recruitment at Various Mucosal Sites in Mouse: An Integrative Analysis
title_fullStr Route of Sensitization to Peanut Influences Immune Cell Recruitment at Various Mucosal Sites in Mouse: An Integrative Analysis
title_full_unstemmed Route of Sensitization to Peanut Influences Immune Cell Recruitment at Various Mucosal Sites in Mouse: An Integrative Analysis
title_short Route of Sensitization to Peanut Influences Immune Cell Recruitment at Various Mucosal Sites in Mouse: An Integrative Analysis
title_sort route of sensitization to peanut influences immune cell recruitment at various mucosal sites in mouse an integrative analysis
topic food allergy
peanut
routes of exposure
BALB/c mice
cellular immune response
url https://www.mdpi.com/2072-6643/14/4/790
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